TY - JOUR
T1 - Evolution of l-DOPA 4,5-dioxygenase activity allows for recurrent specialisation to betalain pigmentation in Caryophyllales
AU - Sheehan, Hester
AU - Feng, Tao
AU - Walker-Hale, Nathanael
AU - Lopez-Nieves, Samuel
AU - Pucker, Boas
AU - Guo, Rui
AU - Yim, Won C.
AU - Badgami, Roshani
AU - Timoneda, Alfonso
AU - Zhao, Lijun
AU - Tiley, Helene
AU - Copetti, Dario
AU - Sanderson, Michael J.
AU - Cushman, John C.
AU - Moore, Michael J.
AU - Smith, Stephen A.
AU - Brockington, Samuel F.
N1 - Funding Information:
We thank two anonymous reviewers for their comments. We thank Hiroshi Maeda, Ya Yang, Fernando Gandía‐Herrero and Joseph Walker for critical reading of the manuscript, Fernando Gandía‐Herrero for providing the betanin standard, and Syngenta for providing the YTiBv seeds. We thank Cambridge University Botanic Garden for growing various species included in this study, the Desert Botanical Garden for access to Aizoaceae samples, and Kevin Thiele for the provision of seed. We acknowledge support from the following funding bodies: SFB, BBSRC High Value Chemicals from Plants Network; HS, SNF P2BEP3_165359 & P300PA_174333; TF, U1802232 & XDA20050203; NWH, Woolf Fisher Cambridge Scholarship; MJM, NSF DEB 1352907; SS, NSF DEB 1354048; JCC, DOE, GSP DE‐SC0008834; RG, CSC no. (2018) 3101. B. vulgaris Macarthuria australis
Funding Information:
We thank two anonymous reviewers for their comments. We thank Hiroshi Maeda, Ya Yang, Fernando Gandía-Herrero and Joseph Walker for critical reading of the manuscript, Fernando Gandía-Herrero for providing the betanin standard, and Syngenta for providing the B. vulgaris YTiBv seeds. We thank Cambridge University Botanic Garden for growing various species included in this study, the Desert Botanical Garden for access to Aizoaceae samples, and Kevin Thiele for the provision of Macarthuria australis seed. We acknowledge support from the following funding bodies: SFB, BBSRC High Value Chemicals from Plants Network; HS, SNF P2BEP3_165359 & P300PA_174333; TF, U1802232 & XDA20050203; NWH, Woolf Fisher Cambridge Scholarship; MJM, NSF DEB 1352907; SS, NSF DEB 1354048; JCC, DOE, GSP DE-SC0008834; RG, CSC no. (2018) 3101.
Publisher Copyright:
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust
PY - 2020/8/1
Y1 - 2020/8/1
N2 - The evolution of l-DOPA 4,5-dioxygenase activity, encoded by the gene DODA, was a key step in the origin of betalain biosynthesis in Caryophyllales. We previously proposed that l-DOPA 4,5-dioxygenase activity evolved via a single Caryophyllales-specific neofunctionalisation event within the DODA gene lineage. However, this neofunctionalisation event has not been confirmed and the DODA gene lineage exhibits numerous gene duplication events, whose evolutionary significance is unclear. To address this, we functionally characterised 23 distinct DODA proteins for l-DOPA 4,5-dioxygenase activity, from four betalain-pigmented and five anthocyanin-pigmented species, representing key evolutionary transitions across Caryophyllales. By mapping these functional data to an updated DODA phylogeny, we then explored the evolution of l-DOPA 4,5-dioxygenase activity. We find that low l-DOPA 4,5-dioxygenase activity is distributed across the DODA gene lineage. In this context, repeated gene duplication events within the DODA gene lineage give rise to polyphyletic occurrences of elevated l-DOPA 4,5-dioxygenase activity, accompanied by convergent shifts in key functional residues and distinct genomic patterns of micro-synteny. In the context of an updated organismal phylogeny and newly inferred pigment reconstructions, we argue that repeated convergent acquisition of elevated l-DOPA 4,5-dioxygenase activity is consistent with recurrent specialisation to betalain synthesis in Caryophyllales.
AB - The evolution of l-DOPA 4,5-dioxygenase activity, encoded by the gene DODA, was a key step in the origin of betalain biosynthesis in Caryophyllales. We previously proposed that l-DOPA 4,5-dioxygenase activity evolved via a single Caryophyllales-specific neofunctionalisation event within the DODA gene lineage. However, this neofunctionalisation event has not been confirmed and the DODA gene lineage exhibits numerous gene duplication events, whose evolutionary significance is unclear. To address this, we functionally characterised 23 distinct DODA proteins for l-DOPA 4,5-dioxygenase activity, from four betalain-pigmented and five anthocyanin-pigmented species, representing key evolutionary transitions across Caryophyllales. By mapping these functional data to an updated DODA phylogeny, we then explored the evolution of l-DOPA 4,5-dioxygenase activity. We find that low l-DOPA 4,5-dioxygenase activity is distributed across the DODA gene lineage. In this context, repeated gene duplication events within the DODA gene lineage give rise to polyphyletic occurrences of elevated l-DOPA 4,5-dioxygenase activity, accompanied by convergent shifts in key functional residues and distinct genomic patterns of micro-synteny. In the context of an updated organismal phylogeny and newly inferred pigment reconstructions, we argue that repeated convergent acquisition of elevated l-DOPA 4,5-dioxygenase activity is consistent with recurrent specialisation to betalain synthesis in Caryophyllales.
KW - Caryophyllales
KW - anthocyanins
KW - betalains
KW - convergent evolution
KW - gene duplication
KW - l-DOPA 4, 5-dioxygenase (DODA)
KW - metabolic operon
KW - plant pigments
KW - specialised metabolism
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UR - http://www.scopus.com/inward/citedby.url?scp=85073991968&partnerID=8YFLogxK
U2 - 10.1111/nph.16089
DO - 10.1111/nph.16089
M3 - Article
C2 - 31369159
AN - SCOPUS:85073991968
VL - 227
SP - 914
EP - 929
JO - New Phytologist
JF - New Phytologist
SN - 0028-646X
IS - 3
ER -